Nonhepathic origin of notothenioid antifreeze reveals pancreatic synthesis as common mechanism in polar fish freezing avoidance. Proc Natl Acad Sci USA

Department of Animal Biology, University of Illinois, Urbana, IL 61801, USA.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 08/2006; 103(27):10491-6. DOI: 10.1073/pnas.0603796103
Source: PubMed


Phylogenetically diverse polar and subpolar marine teleost fishes have evolved antifreeze proteins (AFPs) or antifreeze glycoproteins (AFGPs) to avoid inoculative freezing by internalized ice. For over three decades since the first fish antifreeze (AF) protein was discovered, many studies of teleost freezing avoidance showed hepatic AF synthesis and distribution within the circulation as pivotal in preventing the blood, and therefore the fish, from freezing. We have uncovered an important twist to this long-held paradigm: the complete absence of liver synthesis of AFGPs in any life stage of the Antarctic notothenioids, indicating that the liver plays no role in the freezing avoidance in these fishes. Instead, we found the exocrine pancreas to be the major site of AFGP synthesis and secretion in all life stages, and that pancreatic AFGPs enter the intestinal lumen via the pancreatic duct to prevent ingested ice from nucleating the hyposmotic intestinal fluids. AFGPs appear to remain undegraded in the intestinal milieu, and the composition and relative abundance of intestinal AFGP isoforms are nearly identical to serum AFGPs. Thus, the reabsorption of intact pancreas-derived intestinal AFGPs, and not the liver, is the likely source of circulatory AFGPs in notothenioid fishes. We examined diverse northern fish taxa and Antarctic eelpouts with hepatic synthesis of bloodborne AF and found that they also express secreted pancreatic AF of their respective types. The evolutionary convergence of this functional physiology underscores the hitherto largely unrecognized importance of intestinal freezing prevention in polar teleost freezing avoidance, especially in the chronically icy Antarctic waters.

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    • "The impacts of low temperatures and seasonally limited food availability have long been recognized as primary selective forces driving the evolution of the many endemic species found in Antarctica today [4-8]. In addition to the high degree of endemism produced by these evolutionary processes, a wide-array of functional adaptations have been fixed among protein families of several Antarctic fish, including chaperonins [9], heat shock proteins [10,11], heme proteins [12,13], tubulin kinetics [14], and anti-freeze proteins [15,16]. This rigid oceanographic stability however, may have resulted in an ecosystem filled with endemic fauna that are poorly poised to deal with rapid climate variation [7,17]. "
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    ABSTRACT: The notothenioids comprise a diverse group of fishes that rapidly radiated after isolation by the Antarctic Circumpolar Current approximately 14--25 million years ago. Given that evolutionary adaptation has led to finely tuned traits with narrow physiological limits in these organisms, this system provides a unique opportunity to examine physiological trade-offs and limits of adaptive responses to environmental perturbation. As such, notothenioids have a rich history with respect to studies attempting to understand the vulnerability of polar ecosystems to the negative impacts associated with global climate change. Unfortunately, despite being a model system for understanding physiological adaptations to extreme environments, we still lack fundamental molecular tools for much of the Nototheniidae family. Specimens of the emerald notothen, Trematomus bernacchii, were acclimated for 28 days in flow-through seawater tanks maintained near ambient seawater temperatures (-1.5[degree sign]C) or at +4[degree sign]C. Following acclimation, tissue specific cDNA libraries for liver, gill and brain were created by pooling RNA from n = 5 individuals per temperature treatment. The tissue specific libraries were bar-coded and used for 454 pyrosequencing, which yielded over 700 thousand sequencing reads. A de novo assembly and annotation of these reads produced a functional transcriptome library of T. bernacchii containing 30,107 unigenes, 13,003 of which possessed significant homology to a known protein product. Digital gene expression analysis of these extremely cold adapted fish reinforced the loss of an inducible heat shock response and allowed the preliminary exploration into other elements of the cellular stress response. Preliminary exploration of the transcriptome of T. bernacchii under elevated temperatures enabled a semi-quantitative comparison to prior studies aimed at characterizing the thermal response of this endemic fish whose size, abundance and distribution has established it as a pivotal species in polar research spanning several decades.The comparison of these findings to previous studies demonstrates the efficacy of transcriptomics and digital gene expression analysis as tools in future studies of polar organisms and has greatly increased the available genomic resources for the suborder Notothenioidei, particularly in the Trematominae subfamily.
    BMC Genomics 11/2013; 14(1):805. DOI:10.1186/1471-2164-14-805 · 3.99 Impact Factor
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    • "Убедительно говорят об этом примеры гетеротопного параллелизма как на видовом (фии логенетическом) уровне организации (независии мое сходство молекул у тресковых в Арктике и ноо тотениевидных в Антарктике и, возможно, в разз ных филогенетических ветвях Notothenioidei (Chen et al., 1997; Matschiner et al., 2011)), так и на организменном (онтогенетическом) уровне (синн тез молекул у тресковых и в желудочноокишечч ном тракте, и в печени). Хотя в последнем аспекте нототениевидные рыбы кажутся исключением, поскольку у них синтез гликопротеинов в печени не подтверждён (Cheng et al., 2006), но обнаружее ние гликопротеинов в их кожной слизи свидее тельствует о наличии у этих рыб гетеротопного синтеза AFGP. В геноме нототениевидных могут быть разные копии генов AFGP, подобно тому, что, например, имеет место с генами AFP типа I у американской, или зимней, камбалы Pseudopleuu ronectes americanus. "
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    ABSTRACT: A new species of plunderfish Pogonophryne favosa sp. n. from the mesobenthal of the Cosmonauts Sea, Antarctica, has been described. The new species belongs to a group of species “mentella”, differing from other species of the group in the presence of spots on the abdominal side of the body and a unique structure of mental barbel. An anatomohistological study was performed of convexitas superaxillaris—unusual skin formations first found in Artedidraconidae. Their possible function in the system of cold resistance of Antarctic Notothenioidei and possible historic dates of their appearance in the family Artedidraconidae are discussed.
    Journal of Ichthyology 09/2013; 53(8). DOI:10.1134/S0032945213050020
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    • "In this study we focus on the Antarctic notothenioids, a suborder of marine perciform fishes that represent an example of adaptive radiation in an extreme environmental setting (Eastman and McCune 2000; Matschiner et al. 2011; Rutschmann et al. 2011; Lau et al. 2012). Antarctic notothenioids are endemic to the Southern Ocean, the world's coldest and iciest marine waters (Dayton et al. 1969; Hunt et al. 2003; Cheng et al. 2006). Together with the purely Antarctic Nototheniidae, Harpagiferidae, Bathydraconidae, Artedidraconidae, and Channichthyidae, the clade also includes the three ancestral families Bovichtidae, Pseudaphritidae, and Eleginopidae, represented by 11 mainly non-Antarctic species. "
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    ABSTRACT: To assess how ecological and morphological disparity is interrelated in the adaptive radiation of Antarctic notothenioid fish we used patterns of opercle bone evolution as a model to quantify shape disparity, phylogenetic patterns of shape evolution, and ecological correlates in the form of stable isotope values. Using a sample of 25 species including representatives from four major notothenioid clades, we show that opercle shape disparity is higher in the modern fauna than would be expected under the neutral evolution Brownian motion model. Phylogenetic comparative methods indicate that opercle shape data best fit a model of directional selection (Ornstein-Uhlenbeck) and are least supported by the "early burst" model of adaptive radiation. The main evolutionary axis of opercle shape change reflects movement from a broad and more symmetrically tapered opercle to one that narrows along the distal margin, but with only slight shape change on the proximal margin. We find a trend in opercle shape change along the benthic-pelagic axis, underlining the importance of this axis for diversification in the notothenioid radiation. A major impetus for the study of adaptive radiations is to uncover generalized patterns among different groups, and the evolutionary patterns in opercle shape among notothenioids are similar to those found among other adaptive radiations (three-spined sticklebacks) promoting the utility of this approach for assessing ecomorphological interactions on a broad scale.
    Ecology and Evolution 09/2013; 3(9):3166-3182. DOI:10.1002/ece3.708 · 2.32 Impact Factor
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